A snapshot of a representative Brazilian state of illegal mining in indigenous areas during the era of malaria elimination

Abstract: Malaria is a public health problem and the cases diagnosed in the capital of Roraima, Brazil, show potential to characterize the burden of the disease in the state. This study aimed to describe the epidemiological, clinical, and laboratory aspects of malaria cases diagnosed in Boa Vista. For this purpose, a descriptive, cross-sectional study was conducted in two health units in the city, with individuals diagnosed and who agreed to respond the questionnaire. Of the total of 206 participants, characterized as men, mixed-race, and young, 96% (198) reported participating in illegal mining activity. Among the group of miners, 66% (131) came from other states of Brazil or other countries. The mines were mainly located in the Yanomami territory in Roraima. Plasmodium vivax infection occurred in 74% (153) of participants. In the miner’s group, hospitalizations for severe malaria, previous malaria attacks, and delays in treatment after the onset of symptoms were reported. Although 73% (145) of miners reported knowing how malaria was transmitted, only 54% (107) used mosquito nets or repellents. The use of Artecom and chloroquine by miners is not for the complete treatment but only to relieve symptoms for returning to gold mines, highlighting the importance of molecular surveillance to antimalarial resistance. Indigenous peoples are considered vulnerable to malaria and miners promotes the increase of malaria in Roraima Indigenous Lands. Therefore, access to diagnosis and treatment in Indigenous areas invaded by miners is imperative to confront this disease that ravages Indigenous communities and threatens public health on a large scale to achieve the goal of eliminating malaria in the state.


Introduction
Malaria is an acute febrile infectious disease, caused by the protozoan of the genus Plasmodium, transmitted by the female mosquito of the genus Anopheles 1,2 .The disease is endemic in 85 countries (including the territory of French Guiana) located in tropical and subtropical regions of the world.In 2022, 249 million malaria cases and 608,000 deaths were estimated.In the Americas region, Venezuela, Brazil, and Colombia accounted for more than 73% of the 0.6 million cases that occurred in this region 2 .
In Brazil, malaria is endemic in the Legal Amazon (Acre, Amapá, Amazonas, Maranhão, Mato Grosso, Pará, Rondônia, Roraima, and Tocantins states), which accounts for 99% of cases of the disease in the country.In 2021, 139,107 malaria cases and 61 deaths were recorded in the country 3 .That same year, Roraima presented 26,005 autochthonous cases and 25 deaths from the disease 4 .
Despite being a preventable and treatable disease with medicines available free of charge in the Brazilian Unified National Health System (SUS, acronym in Portuguese), morbidity and mortality data show that malaria is still an important public health problem.The disease negatively impacts both the health and livelihoods of people worldwide, especially the poorest and most vulnerable populations.Moreover, it poses challenges for its elimination, demanding successful strategies to achieve the goal of eliminating malaria transmission in Brazil by 2035 5 .
From 2010 to 2020, the period that precedes the decade of work for Brazil to achieve the elimination target, cases of malaria imported from Venezuela and mining in the Yanomami Indigenous area were identified as the factors responsible for the increase in cases of the disease in Roraima 6 .The diagnosis of malaria occurred mainly in Boa Vista, the state capital.In this scenario, in addition to the clear impact on the municipal healthcare network, there is also the risk of outbreaks and epidemics in Boa Vista.In fact, the municipality shows a climate favorable to the main vectors of malaria, along with large rivers, streams, and lakes in the urban area of the city, characteristics that also favor the existence of breeding sites 7 .
The health units with the highest number of case notifications were the Cosme e Silva Emergency Service Unit and the Sayonara Maria Dantas Basic Health Unit, representing 31% (4,490) and 14% (2,075) of cases, respectively, accounting for almost 50% of the malaria cases notified in Boa Vista 8 .
In the group of individuals seeking a malaria diagnosis in Boa Vista, it is possible to identify multiple factors that can characterize the epidemiological pattern of the malaria burden in the state of Roraima, which can support the formulation of effective public policies to control malaria disease following local reality 9 .
Mining activity is allowed by law in Brazil.However, mining activities in the Amazon are mostly operated without a license, with mercury, within Indigenous Lands and Conservation Units, and without environmental recovery efforts.Such mining activities are considered illegal.
Given the representativeness of malaria cases diagnosed in Boa Vista, the objective of this work was to investigate where the infection occurs and the main activity of infected individuals via an epidemiological survey.Moreover, we investigated the clinical and laboratory aspects of malaria cases reported in the two units that concentrate the largest number of malaria notifications.

Methodology
The state of Roraima, located in the extreme north of Brazil, shares an international border with Venezuela and Guyana, as well as a national border with the states of Amazonas and Pará.In 2021, according to the Brazilian Institute of Geography and Statistics (IBGE, acronym in Portuguese) 10  Roraima held a population of 652,713 inhabitants.The state capital, Boa Vista, concentrates 67% of the population, with 436,591 inhabitants, and is bordered by the municipalities of Pacaraima, Normandia, Bonfim, Cantá, Mucajaí, Alto Alegre, and Amajari (Figure 1).It comprises 15 municipalities and 104,509.087km 2 of its territory consists of Indigenous reservations.The Yanomami Indigenous Land is the largest Indigenous reserve in Brazil.The Special Indigenous Health District Yanomami (DSEI-Yanomami) in Roraima covers five municipalities: Alto Alegre, Amajari, Caracaraí, Iracema, and Mucajaí.All mining sites in Roraima are illegal and located within Indigenous Lands, and the largest of them are in Yanomami territories.
Boa Vista holds 15 malaria diagnostic centers located in the urban area of the city, six in hospital/ urgency and emergency units; one in maternal and child hospital; and eight in primary health care (PHC) units.The study was conducted in two health units located in the west of Boa Vista: the Cosme e Silva Emergency Service Unit and the Sayonara Maria Dantas Basic Health Unit (Figure 1).These notification units were chosen due to holding the highest number of malaria notifications in Boa Vista, according to SIVEP-Malaria.
To achieve the proposed objective, a descriptive, cross-sectional study was conducted from December 2021 to June 2022, during the driest season of the year in Roraima, when malaria transmission is favored, consequently leading to an increase in diagnosis demand.Individuals over 18 years of age and diagnosed with malaria via thick blood smears were included in the study.Minors under 18 years of age, Indigenous people living in villages, those who were unable to read the informed consent form, and individuals who refused to sign it did not participate.
This work was approved by the Research Ethics Committee of the Federal University of Roraima (CEP/UFRR, acronym in Portuguese; opinion n. 3,920,373, issued on March 17, 2020).The CEP/ UFRR allowed only the inclusion of non-village Indigenous people who speak Brazilian Portuguese and reside in Boa Vista.Additionally, the research project was demanded to be presented to the Kannu Kadan Indigenous Association for obtaining a letter of consent which was attached in the submission process to the CEP/UFRR.
Participants signed an informed consent form before responding a questionnaire containing questions related to the individual (gender, age, ethnicity, place of residence, main activity in the 15 days before the onset of symptoms, knowledge about the forms of malaria transmission, and prophylaxis) and the disease (symptoms, parasitic form causing the infection, and history of the disease).The questionnaires were typed and tabulated in the Excel software (https://products.office.com/).
The maps were created using the QGIS program version 3.28.10(https://qgis.org/en/site/), and mining areas in Roraima were obtained from MapBiomas 11 .Geopolitical limits of Brazil and Indigenous Lands were accessed on the IBGE website 12 .

Results
According to SIVEP-Malaria, during the study period (December 2021 to June 2022), 7,379 malaria cases were notified in Boa Vista and 43% of them were diagnosed in the health units selected as strategic points for this research.
When analyzing participants' responses about the main activity performed in the 15 days before the onset of symptoms, four activities were identified.Mining was the predominant activity (p < 0.0001) with 198 (96%) participants, followed by agriculture with 6 (3%), hunting/fishing with 1 (0.5%), and tourism with 1 (0.5%).
The age of the participants ranged from 18 to 67 years old, and the age groups 18 to 29 and 30 to 39 years old were prevalent in participants who reported mining activity (p < 0.0001).Of the total number of participants, men were more frequent than women (p < 0.0001), with 169 (82%) men.Additionally, mixed-race was the most frequent ethnicity, with 119 (58%) individuals (p < 0.0001).Fever (90.3%), headache (87.4%), chills (67.5%), abdominal pain (54.9%), and myalgia (53.4%) were found to be more predominant symptoms compared to sweating, diarrhea, dyspnea, low back pain, and no symptoms (p < 0.0001).In total, 202 participants (98%) reported at least one symptom.The same symptomology was described by the miners, being the only group with asymptomatic participants (four in total, accounting for 2%) (Table 1).
The nonuse of prophylactic measures and the use of repellent were the most cited when asked about prophylactic measures (p < 0.0001).Moreover, only the miners' group reported using antimalarials as a form of prophylaxis, with 14 (6%) reports (Table 1).
Concerning the timeliness of treatment, starting treatment within 96 hours and after 96 hours were more frequent than other periods, that is, up to 24 or 48 hours (p = 0.0024) and 57 (29.4%) miners started treatment after 96 hours since the onset of symptoms (Table 2).
Concerning participants who performed agricultural activities, around 33% (2) came from Roraima and the remaining were from Pará, Amazonas, Bahia, and Venezuela.The participant who performed hunting/fishing occupation was from Pará and the participant who reported working with tourism was from Piauí.

Discussion
This is a descriptive study.We highlight that the selected units are representative of the malariadiagnosed cases in Roraima.Our casuistic comprises cases of passive surveillance/search.Therefore, we may be underestimating the number of cases since individuals who perform self-treatment in mining, without seeking health facilities, could only be identified by active search in mining areas in Yanomami lands.However, this active search is hindered by the location of the mines in remote forest areas whose access is often via clandestine take-off and landing strips, besides the risks to the researchers' lives in these conflict areas.
Identifying the place of infection is essential to guide the planning of malaria prevention and control actions.In Brazil, cases of malaria in urban and rural areas and settlements have decreased since 2017, contrasting with cases in miners and Indigenous people, which increased around 257% and 62%, respectively 6,14 .
In this study, 96% of the participants reported mining activity at least 15 days before the onset of symptoms, strongly suggesting that they were infected in Indigenous Lands where all Roraima illegal mines are located.

Table 2
Characterization of the case series by the main activity conducted 15 days before the onset of symptoms, according to the period of initiation of treatment after the appearance of symptoms.Boa Vista, state of Roraima, Brazil.The presence of miners in the Yanomami Indigenous territories contributed to the increased number of malaria cases in Roraima in recent years.Even in 2020, during the COVID-19 pandemic, there was a 44% increase in autochthonous malaria cases in Roraima and in the Yanomami Indigenous Land, which corresponds to a 77% increase when compared to 2019, disregarding the increased number of hospitalizations and deaths.In this same period, a 30% increase in mining activity was also noted in the Yanomami Indigenous area 6 .The mines are very close to the Indigenous communities.The Uraricoera River concentrated 52% of the entire area degraded by mining; gold exploration takes place in the Waikás, Araçá, and Korekorema Indigenous communities.The mines along the Mucajaí River (and its tributary Couto de Magalhães) represent almost 25% of the total mining activities; gold exploration occurs in the borders of the Kayanau and Papiu Indigenous communities 15 .

Onset of symptoms
Indigenous reserves are considered the most preserved areas and are responsible for forest conservation 16 .The mining activity in Yanomami Indigenous Land has multiple impacts on traditional communities and the ecosystem 16 .Disintrusion is necessary, but it is not a simple or low-cost process.In this context, a robust political, economic, and public security project must be developed.Evidence of the presence of organized crime (called narco mining) makes the process even more difficult 16,17 , as well as health actions to control malaria in these areas.

Figure 2
Municipalities of infection of participants who carried out mining activities 15 days before the onset of symptoms.Boa Vista, state of Roraima, Brazil.
Source: prepared by the authors.

Figure 3
Origin of study participants who carried out illegal mining activity 15 days before diagnosis.Boa Vista, state of Roraima, Brazil.
Source: prepared by the authors.
Mining is a major challenge for the elimination of malaria over the next decade in Brazil.In addition to requiring health and environmental interventions, there is a need to formulate control policies that include the specificity of the garimpeiro population, despite the illegality of mining activity 6,14,18 since controlling malaria in this population can reduce the impact of malaria on Indigenous people.
Miners can increase malaria transmission via three main factors: (a) modification of the environment, with the use of hoses and combustion engines to extract the sediment, forming pools of water that serve as breeding grounds, enhancing the reproduction of the mosquito vector, especially A. darlingi; (b) more exposition to mosquitoes by work outdoors for long periods a day and sleep in tents Cad.Saúde Pública 2024; 40(6):e00224023 with incomplete walls; and (c) the intense mobility between the mining areas and their place of residence or other areas, promoting transmission and the occurrence of outbreaks 19,20,21,22 .
The number of women in mining activity, although smaller, should also be considered for strategies to eliminate malaria, especially due to the possibility of pregnancy, as severe malaria disease, when not treated promptly, can lead to conditions such as, maternal and fetal anemia; premature birth; low birth weight and fetal problems; and maternal and neonatal death 23,24,25 .
Fever, followed by headache, was the most frequent symptom among study participants.Fever remains the main symptom for health education strategies on the identification of malaria symptoms.Therefore, the advice to seek a health unit if one is feeling feverish and has been in an area at risk for malaria transmission continues to be an important guideline for timely diagnosis and treatment.We highlight that cultural differences must be considered so that this strategy is effective, especially in territories with multi-ethnic borders 26,27 .
In the group of miners, 81% (161) had previous malaria attacks and 2% (4) had no symptoms at the time of diagnosis.It was not possible to define whether previous episodes of malaria were related to relapse, recrudescence, or reinfection.Furthermore, miners reported that soon after the diagnosis and treatment for malaria, they returned to the mine, often on the same day, thus being constantly exposed to areas where malaria is transmitted.
The silent condition of asymptomatic carriers represents a challenge to the elimination of malaria 25,28 ; therefore, surveillance must also track the movement of human carriers.The asymptomatic participants engaged in this study were relatives of the patients who had the malaria diagnosis at Boa Vista.Since they also came from mining areas, the malaria microscopic test was performed.
Regarding the parasitic form, 53 cases of infection by P. falciparum and P. falciparum + P. vivax (mixed malaria) were identified, of which 51 were in miners.In the Americas region, P. vivax malaria represents 75% of cases 22 .However, in mining areas, P. falciparum appears to be more frequent than in other ones 18,28 .Notably, among the 11 cases of mixed P.falciparum/P.vivaxinfections, 10 were in miners.In this context, updating microscopists or adopting more precise diagnostic procedures is crucial for adequate treatment.If mixed infections are misdiagnosed as a P. vivax monoinfection and treatment is prescribed only for this parasite, the increase in P. falciparum parasitemia may evolve into severe malaria 29 .
For miners, absenteeism due to malaria causes a major financial impact.Thus, self-medication and the use of sub-doses of medication as a form of prophylaxis or quick relief of symptoms are common in this group 21,30 .In the national malaria treatment protocol, chloroquine is the first-line treatment for uncomplicated malaria caused by P. vivax.A combination of chloroquine is prescribed for three days (10mg/kg on day 1 and 7.5mg/kg on days 2 and 3) and primaquine (0.5mg/kg/day, for seven days), aiming to cure both the blood form and the hepatic form (radical cure), respectively, thus avoiding relapse due to hypnozoites 31 .However, the medication used by the miners who participated in this study was Artecon, which could be purchased at the mine itself.This drug is not recommended by local pharmaceutical authorities and the World Health Organization and it is illegal in Brazil, French Guiana, and neighboring countries 28,32 .
In this way, the increase in the number of infections, in addition to the emergence of resistance to antimalarials could occur, reinforcing the need for molecular surveillance via antimalarial resistance markers in mining areas, especially in the case of artemisinin 18,33,34,35 .
The Brazilian National Malaria Control Program considers treatment with antimalarials to be opportune when it is conducted within 48 hours from the onset of symptoms for autochthonous cases and within 96 hours for imported cases 5 .However, most miners reported starting treatment after 96 hours or more.In this study, in the group of miners, 29% (57) were diagnosed after 96 hours.
In this scenario, it is important to introduce diagnosis and treatment in mining to interrupt the transmission and, consequently, reduce the burden of malaria in Indigenous areas.However, in Roraima, given the illegality of mining activity together with the narco mining 17 , healthcare teams are unsafe to perform diagnosis and treatment in mining areas.
The Malakit Project was a successful and innovative strategy with an impact on the reduction of malaria cases in miner populations in French Guiana and Suriname.This intervention proposed to provide miners with training on malaria, kits for self-diagnosis via rapid testing, and self-treatment Cad.Saúde Pública 2024; 40(6):e00224023 32,36 .In Roraima, this strategy could be adopted at health units diagnosing malaria in miners to overcome lack of security in conflict areas.
Notably, 66% of the miners in this study came from other Brazilian areas, including those of the extra-Amazonian region, or Venezuela.The mobility of miners is a challenge to eliminating malaria since infected people cross borders and increase the possibility of reintroducing malaria into areas where malaria has been reduced or eliminated, as well as spreading malaria parasites 34,35,37 .

Conclusion
The snapshot of malaria diagnosed in Boa Vista shows that the burden of malaria transmission in the state occurs in the mines located in the Yanomami Indigenous Land.The presence of miners increases the number of malaria cases in Roraima, including in its Indigenous reserve.
The disintrusion of miners from Yanomami territories is urgently needed and requires a robust and complex long-term government project.Meanwhile, public health in Brazil can conduct strategies to control malaria among miners to protect the Indigenous peoples and decrease the transmission in Roraima.These strategies can aid reducing malaria cases in the Yanomami Indigenous population and, consequently, achieving the goal of eliminating malaria by 2035.To this end, surveillance must be also implemented with cooperative policies between municipalities and federal units in Brazil and neighboring countries to detect the mobility routes of garimpeiro populations.

Figure 1
Figure 1Location of the municipality of Boa Vista, state of Roraima, Brazil, showing the urban area, rivers networks and streams, and malaria diagnostic units.

Table 1
Characterization of study subjects, according to the main activity performed 15 days before by age group, gender, ethnicity, symptoms, parasitic species, and epidemiological variables related to malaria.Boa Vista, state of Roraima, Brazil.